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DOI: 10.1055/s-0034-1392533
A randomized comparison of cold snare polypectomy versus a suction pseudopolyp technique
Corresponding author
Publication History
submitted 05 December 2014
accepted after revision 28 May 2015
Publication Date:
10 July 2015 (online)
Background: Cold snare techniques are widely used for removal of diminutive and small colorectal polyps. The influence of resection technique on the effectiveness of polypectomy is unknown. We therefore compared standard cold snare polypectomy with a newly described suction pseudopolyp technique, for completeness of excision and for complications.
Patients and methods: In this single-center study, 112 patients were randomized to cold snare polypectomy or the suction pseudopolyp technique. Primary outcome was endoscopic completeness of excision. Consensus regarding the endoscopic assessment of completeness of excision was standardized and aided by chromoendoscopy. Secondary outcomes included: completeness of histological excision, polyp “fly away” and retrieval rates, early bleeding (48 hours), delayed bleeding (2 weeks), and perforation.
Results: 148 polyps were removed, with size range 3 – 7 mm, 60 % in the left colon, and 90 % being sessile. Regarding completeness of excision (with uncertain findings omitted): endoscopically, this was higher with the suction pseudopolyp technique compared with cold snare polypectomy but not statistically significantly so (73/74 [98.6 %] vs. 63/68 [92.6 %]; P = 0.08). A trend towards a higher complete histological excision rate with the suction pseudopolyp technique was also not statistically significant (45/59 [76.3 %] vs. 37/58 [63.8 %]; P = 0.14). Polyp retrieval rate was not significantly different (suction 68/76 [89.5 %] vs. cold snare 64/72 [88.9 %]; P = 0.91). No perforation or bleeding requiring hemostasis occurred in either group.
Conclusion: In this study both polypectomy techniques were found to be safe and highly effective, but further large multicenter trials are required.
Clinical trial registration at www.clinicaltrials.gov: NCT02208401
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Introduction
It is widely accepted that colonoscopic polypectomy reduces the incidence and mortality of colorectal cancer by disrupting the polyp-cancer sequence. However, the vast majority of polyps encountered during routine colonoscopy are diminutive (1 – 5 mm) or small (6 – 9 mm) and 9 % – 10 % will have advanced histology [1] [2]. It is not known which of these polyps will progress to cancer so all are removed.
Several polypectomy techniques are available for the removal of small polyps, with the choice of technique influenced by the size, site, and morphology of the polyp and the practice of the colonoscopist. Many advocate the use of a cold snare for the removal of diminutive and small polyps since it avoids diathermy-associated complications. However, incomplete resection rates of 7 % – 21 % have been reported with cold snare techniques [3] [4] [5] [6].
In an attempt to improve completeness of resection, Pattullo et al. described a novel method, the pseudopolyp technique, for the removal of small polyps and achieved complete endoscopic resection rates of 100 % without any immediate or delayed complications [7]. These impressive results, however, were non-comparative and no assessment was made of the histological completeness of excision.
We have therefore undertaken a randomized comparison of the suction pseudopolyp technique and standard cold snare polypectomy and incorporated an assessment of the histological completeness of excision.
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Method
Study population and design
The study was a single-center, prospective randomized controlled trial of outpatients undergoing routine diagnostic colonoscopy between January 2014 and August 2014. The study protocol was approved by the local research ethics committee and was performed in compliance with the Helsinki Declaration. The trial was reported according to the Consolidated Standards of Reporting Trials (CONSORT) guidelines and was registered at www.clinicaltrials.gov (NCT02208401). Written informed consent was obtained from all patients including for recording the procedure and for telephone follow-up.
Patients over the age of 18 years who were found to have one or more sessile or flat polyps measuring 3 – 7 mm were considered eligible. Cold snaring is recommended for polyps in this size range [8] [9] [10] and they are more amenable to the suction pseudopolyp technique because of the size limitation of the colonoscope suction channel. Those taking antiplatelet agents (except aspirin) or anticoagulant therapy were excluded. Also excluded were patients with polyps identified that were behind folds thus making it difficult to endoscopically assess completeness of excision.
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Randomization and concealment
Patients were randomly assigned in a 1:1 ratio to the suction pseudopolyp technique or cold snare polypectomy. The website www.random.org was used to generate a randomization sequence that was concealed by placing the assignments in completely opaque, sequentially numbered envelopes. When an eligible polyp was identified during the procedure, a nurse opened the envelope to reveal the polypectomy technique. If more than one eligible polyp was encountered in the same patient, polypectomies were carried out using the same technique.
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Standardization of assessment of completeness of endoscopic excision
Prior to the study, five participating endoscopists viewed 20 video clips of cold snare polypectomy and the mucosal defect, before and after the defect was sprayed with indigo carmine dye. This process was completed over two rounds in order to establish the criteria for the assessment of completeness of endoscopic resection. Completeness of excision was classified as follows: “complete” (no evidence of residual tissue at the excision margin or polyp base); “incomplete” (any evidence of residual tissue at the excision margin or polyp base) or “uncertain” ([Fig. 1]).
Through the two rounds of the consensus process, the multirater kappa agreements were 0.49 (95 % confidence interval [95 %CI] 0.27 – 0.70) and 0.51 (95 %CI 0.32 – 0.71), suggesting a moderate level of agreement in the endoscopic assessment of completeness of excision.
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Polypectomy protocol
Patients were prescribed standard bowel preparation with either Picolax (Ferring) or Klean-Prep (Norgine). Three experienced endoscopists, from among the five who had established the kappa values, performed the procedures using Olympus CF 260 colonoscopes (Olympus Medical Systems, Tokyo, Japan). All polyps were removed using the Exacto mini snare (US Endoscopy, Mentor, Ohio, USA) without diathermy. Prior to polypectomy, polyp size, site, and morphology were noted. Polyps were sized using the biopsy forceps as a guide (closed diameter 2.4 mm, fully open jaw tips 8 mm; 1332 – 40; Boston Scientific). When the polyp margin was not clearly apparent, the site was sprayed with dilute indigo carmine (0.1 %) prior to polypectomy.
Conventional cold snare polypectomy was performed as follows: (i) slight deflation of luminal air; (ii) excision of polyp, without tenting, in the 5 – 8-o’clock position with the aim of capturing a margin of normal mucosa.
The suction pseudopolyp technique was performed according to the method described by Pattullo et al. [7]: (i) slight deflation of luminal air; (ii) passage of snare down the working channel of the colonoscope until it was 15 – 20 cm from the end of the colonoscope; (iii) center of polyp aligned with the suction channel; (iv) polyp aspirated into the suction channel and continuous suction applied whilst the colonoscope was gently pulled backwards for a distance of 2 – 5 cm; (v) suction released, allowing the colonic wall to spring back with the formation of a pseudopolyp; (vi) cold snare excision of the pseudopolyp, done rapidly before the polyp could resume its original shape.
Polyps were retrieved by suctioning through the biopsy channel of the colonoscope into a polyp trap. The polypectomy site was then visually assessed in real time by the endoscopists for any evidence of residual tissue, by washing the site with water, ensuring good luminal distension and applying 0.1 % indigo carmine ([Fig. 1]). When excision was judged to be incomplete or uncertain, targeted biopsies were taken from areas of residual tissue, the margin, and the base, using large capacity biopsy forceps.
All samples were sent in separate pots to an expert pathologist who was blinded to the polypectomy technique used and endoscopic findings. The criteria for confirming completeness of histological excision were based on the English National Health Service (NHS) Bowel Cancer Screening Programme pathology guidelines [11] and were defined by the absence of residual tissue at the resection margin in any dimension ([Fig. 2]).
All patients were followed up by means of a phone call at 48 hours and 2 weeks after the procedure to assess for any complications.
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Study outcomes
The primary outcome was endoscopic completeness of excision. Secondary outcome measures were: completeness of histologic excision; rate of polyp “fly away” (when the polyp does not remain within or adjacent to the polypectomy site); polyp retrieval rate; early bleeding (48 hours); delayed bleeding (2 weeks); and perforation.
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Statistical analysis
The sample size calculation was based on the results of a previous study that reported that 86 % of polyps were completely resected using the cold snare technique [3]. We determined that at least 56 patients per group would be required to compare the two techniques with a significance level alpha 0.05 and statistical power of 0.80 in order to detect a clinically relevant increase in the completeness of resection of at least 14 %.
Categorical variables were compared using the χ 2 test or Fisher’s exact test, where appropriate. Student’s t test or the Mann-Whitney Wilcoxon test were used for continuous variables. Statistical analysis was performed using SPSS version 20.
Kappa statistics and 95 % confidence intervals were calculated to assess interobserver agreement between the multiple raters [12]. The strength of agreement for a kappa value was classified as: poor, 0.00 to 0.20; fair, 0.21 to 0.40; moderate, 0.41 to 0.60; good, 0.61 to 0.80; and excellent, 0.81 to 1.00 [13].
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Results
Patient flow through the study is summarized in [Fig. 3]. A total of 112 patients (67.9 % men; mean age 63.7 years; range 31 – 86) were found to have at least one sessile or flat polyp measuring 3 – 7 mm and were randomized to undergo polypectomy with the suction pseudopolyp technique (n = 56) or cold snare polypectomy (n = 56). Patient demographic data, indications for colonoscopy, and polyp characteristics were similar between the two groups ([Table 1]).
A total of 148 eligible polyps were detected and 76 were removed using the suction pseudopolyp technique and 72 with cold snare polypectomy. The median polyp size was 4.0 mm, and 89 (60 %) were located in the left colon (distal to and including the splenic flexure) and 125 (84.5 %) were sessile. A total of 132 polyps (89.1 %) were retrieved for histological examination and 13 of those (10 %) had features consistent with advanced pathology, with 12 (92 %) being tubulovillous and 1 (8 %) being a sessile serrated adenoma. No lesion harbored high grade dysplasia or invasive carcinoma.
The overall effectiveness of each polypectomy technique is shown in [Table 2]. For the accurate attribution of completeness of excision, we restricted the analysis to those polyps where excision was judged to be complete or incomplete. Endoscopic completeness of excision was higher with the suction pseudopolyp technique (73/74 [98.6 %, 95 %CI 92.7 % – 100 %]) compared with cold snare polypectomy (63/68 [92.6 %, 95 %CI 83.7 % – 97.6 %]), but this was not statistically significant (P = 0.08). There was also a numerical trend towards a higher complete histological excision rate with the suction pseudopolyp method, but again this difference did not reach statistical significance (45/59 [76.3 %, 95 %CI 63.4 % – 86.3 %] vs. 37/58 [63.8 %, [95 %CI 50.1 – 76.0 %]; P = 0.14). There was no significant difference between the suction pseudopolyp technique and cold snare polypectomy in polyp “fly away” rates (9/76 [11.8 %] vs. 8/72 [11.1 %], respectively; P = 0.89) or retrieval rates (68/76 [89.5 %] vs. 64/72 [88.9 %], respectively; P = 0.91). No immediate or delayed post-polypectomy bleeding requiring endoscopic hemostasis, or other significant complications associated with the techniques, occurred in either group.
|
Suction pseudopolyp technique |
Cold snare polypectomy |
P value |
|
|
Polyps excised, n |
76 |
72 |
|
|
Endoscopic excision |
|||
|
Complete |
0.06[1] |
||
|
n |
73 |
63 |
|
|
% (95 %CI) |
96.1 % (88.9 % – 99.2 %) |
87.5 % (77.6 % – 94.1 %) |
|
|
Incomplete |
|||
|
n |
1 |
5 |
|
|
% (95 %CI) |
1.3 % (0.03 % – 7.2 %) |
6.9 % (2.3 % – 15.5 %) |
|
|
Uncertain |
|||
|
n |
2 |
4 |
|
|
% (95 %CI) |
2.6 % (0.3 % – 9.2 %) |
5.6 % (1.5 % – 13.6 %) |
|
|
Complete rate, omitting “Uncertain” findings |
0.08 |
||
|
n/n |
73/74 |
63/68 |
|
|
% (95 %CI) |
98.6 % (92.7 % – 100 %) |
92.6 % (83.7 % – 97.6 %) |
|
|
Histological excision |
|||
|
Complete |
0.34[1] |
||
|
n |
45 |
37 |
|
|
% (95 %CI) |
59.2 % (47.3 % – 70.4 % |
51.4 % (39.3 % – 63.4 % |
|
|
Incomplete |
|||
|
n |
14 |
21 |
|
|
% (95 %CI) |
18.4 % (10.5 % – 29.0 %) |
29.2 % (19.1 % – 41.1 % |
|
|
Uncertain |
|||
|
n |
17 |
14 |
|
|
% (95 %CI) |
22.4 % (13.6 % – 33.3 %) |
19.4 % (11.1 % – 30.5 %) |
|
|
Complete rate, omitting “Uncertain” findings |
0.14 |
||
|
n/n |
45/59 |
37/58 |
|
|
% (95 %CI) |
76.3 % (63.4 % – 86.3 %) |
63.8 % (50.1 % – 76.0 %) |
|
|
Polyp “fly away” |
0.89 |
||
|
n |
9 |
8 |
|
|
% (95 %CI) |
11.8 % (5.6 % – 21.3 %) |
11.1 % (4.9 % – 20.7 %) |
|
|
Retrieval |
0.91 |
||
|
n |
68 |
64 |
|
|
% (95 %CI) |
89.5 % (80.3 % – 95.3 % |
88.9 % (79.3 % – 95.1 %) |
|
|
Excluded polyps (behind folds), n |
0 |
0 |
|
|
Methods used to prevent bleeding |
None |
None |
|
|
Complications, n |
|||
|
Early bleeding |
0 |
0 |
|
|
Late bleeding |
0 |
0 |
|
|
Perforation |
0 |
0 |
95 %CI, 95 % confidence interval.
1 Comparison between completion rates for the two techniques with the “Uncertain” results included in the total polypectomies.
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Discussion
It has been suggested that the incomplete resection of colorectal polyps may be responsible for up to one third of all interval colorectal cancers [14] [15] [16]. Although this probably relates to larger advanced neoplastic polyps, advanced neoplasia is found in 9 % – 10 % of subcentimeter polyps [1] [2]. It is therefore important that such polyps are removed safely and completely.
Several techniques are available for the removal of diminutive and small colorectal polyps. The cold biopsy technique is often used for the removal of diminutive polyps, but incomplete resection rates of up to 61 % have been reported with standard biopsy forceps [17] and 18 % with jumbo forceps [18]. The hot biopsy technique is sometimes used in the hope of ablating residual tissue, but incomplete removal has been reported in 17 % [19] and the technique is not widely recommended because of the risk of complications and the poor quality of tissue obtained [20] [21].
Alternatively, many endoscopists employ snare techniques with or without diathermy. The hot snare technique achieves higher rates (92 %) of completeness of resection [6], but is associated with a small risk of delayed bleeding and perforation [22] [23].
Cold snare polypectomy is increasingly recommended for the removal of 3 – 7-mm flat and non-bulky sessile polyps [8] [9] [10] and avoids the risk of diathermy-associated complications. Several cohort studies have shown no excess of post-procedural bleeding [1] [22] [23] [24]. The technique aims to remove a 1 – 3-mm margin of normal tissue around the polyp to reduce the risk of recurrence, but incomplete resection rates of up to 21 % have been reported [3] [4] [5] [6]. Since this may be related to inaccurate identification of the polyp margin or imprecise placement of the snare, Pattullo et al. [25] have described a suction pseudopolyp technique, which more readily enables the endoscopist to resect the lesion and a margin of surrounding normal tissue. The technique is simple, quick and easy to learn, and less costly than saline injection techniques.
The present study supports the safety of the suction pseudopolyp technique, but was not powered to detect differences in complications. The retrieval rates in our study are similar to those from other series of cold snare polypectomy [24] [26], but retrieval rates are never likely to be 100 % since small polyps may be lost.
Completeness of histological excision with the suction pseudopolyp technique was much higher in the present study than reported by Pattullo (59.2 % vs. 30 %) [7], but this is likely to reflect differences in study design.
Confirmation of completeness of histological excision can be challenging, as small polyps are more likely to be damaged and to fragment as they pass through the suction channel. Furthermore, the pseudosuction technique may deform the polyp making analysis more difficult. Variations in the mounting process may also make it difficult for the pathologist to assess the polyp margins with certainty. It has therefore been suggested that completeness of resection is best assessed endoscopically at the time of polypectomy [16] [27], but this too can be unreliable [28].
The present study has several strengths. It utilized a randomized controlled design with a standardized chromoendoscopy technique. Konishi et al. report that high resolution chromoendoscopy is just as effective as magnification chromoendoscopy for assessing residual tissue after polypectomy [29]. We also assessed multiple operators to account for the possible variation of technical skills in performing polypectomy.
The study has a number of limitations. First, we did not routinely biopsy the base and margin of all the polypectomy sites, which has been advocated by some [28] [30]. Endoscopic mucosal resection of the polypectomy site has also been employed as a means of assessing completeness of excision and would be considered to be a gold standard method, but may lead to an increased risk of complications. Secondly, we based our power calculation on the published difference in completeness of resection between the two techniques (100 % versus 86 %) [3] [7]. Based on these figures, a rate for endoscopic completeness of resection that is 14 percentage points higher than that of cold snare polypectomy is possible, and this is clearly clinically relevant. In the present study we fell just short of a 100 % rate for complete endoscopic resection with the suction pseudopolyp technique (95 %CI 92.7 % – 100 %), and were unable to demonstrate a significant benefit over standard cold snare polypectomy (95 %CI 83.7 % – 97.6 %) because of our much better than expected performance. To power a study for a 6 % difference in efficacy (the difference in the present study) would require 200 patients per group. A study of this size will take a prolonged period to complete and we believe the present study demonstrates the superiority of the suction pseudopolyp technique over the historically established efficacy of the cold snare method. Thirdly, several polyps were sometimes detected in the same patient, introducing a lack of statistical independence. Finally, since this was an open study, unintended researcher bias may have influenced the results.
In conclusion, both techniques are safe and highly effective for the removal of 3 – 7-mm polyps. Because removal of small polyps is one of the most common endoscopic procedures, an optimal technique should be sought. A larger multicenter trial, including assessment in a blinded fashion of both resection margin biopsies and high quality photos of the polypectomy site would improve generalizability and give a more definite answer as to which technique is best.
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Competing interests: None
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References
- 1 Repici A, Hassan C, Vitetta E et al. Safety of cold polypectomy for < 10 mm polyps at colonoscopy: a prospective multicenter study. Endoscopy 2012; 44: 27-31
- 2 Tsai FC, Strum WB. Prevalence of advanced adenomas in small and diminutive colon polyps using direct measurement of size. Dig Dis Sci 2011; 56: 2384-2388
- 3 Ellis K, Schiele M, Marquis S et al. Efficacy of hot biopsy forceps, cold micro-snare and micro-snare with cautery techniques in the removal of diminutive colonic polyps. Gastrointest Endosc 1997; 45: 329-329
- 4 Humphris JL, Tippett J, Kwok A et al. Cold snare polypectomy for diminutive polyps: an assessment of the risk of incomplete removal of small adenomas. Gastrointest Endosc 2009; 69: AB207
- 5 Lee CK, Shim J-J, Jang JY. Cold snare polypectomy vs. cold forceps polypectomy using double-biopsy technique for removal of diminutive colorectal polyps: a prospective randomized study. Am J Gastroenterol 2013; 108: 1593-1600
- 6 Hyun-Soo K, Hye WonH, Hong JunP et al. Cold snare versus hot snare polypectomy for the complete resection of 5 – 9 mm sized colorectal polyps; A randomised controlled trial. Gastrointest Endosc 2014; 79: AB401-AB402
- 7 Pattullo V, Bourke MJ, Tran KL et al. The suction pseudopolyp technique: a novel method for the removal of small flat nonpolypoid lesions of the colon and rectum. Endoscopy 2009; 41: 1032-1037
- 8 Riley SA. Colonoscopic polypectomy and endoscopic mucosal resection: a practical guide. British Society of Gastroenterology. Available at: http://www.bsg.org.uk/images/stories/docs/sections/endo/polypectomy_08.pdf. Accessed 10 October 2014 2008
- 9 Hewett DG, Rex DK. Colonoscopy and diminutive polyps: hot or cold biopsy or snare? Do I send to pathology? . Clin Gastroenterol Hepatol 2011; 9: 102-105
- 10 Hewett DG. Colonoscopic polypectomy: current techniques and controversies. Gastroenterol Clin North Am 2013; 42: 443-458
- 11 NHS BCS Programme Pathology Group. Reporting lesions in the NHS Bowel Cancer Screening Programme. Guidelines from the Bowel Cancer Screening Programme Pathology Group. NHS BCSP publication no. 1. Sheffield, UK: NHS Cancer Screening Programmes; 2007
- 12 Fleiss JL. Measuring nominal scale agreement among many raters. Psychol Bull 1971; 76: 371-382
- 13 Altman DG. Practical statistics for medical research. London: Chapman and Hall; 1991
- 14 Farrar WD, Sawhney MS, Nelson DB et al. Colorectal cancers found after a complete colonoscopy. Clin Gastroenterol Hepatol 2006; 4: 1259-1264
- 15 Leung K, Pinsky P, Laiyemo AO et al. Ongoing colorectal cancer risk despite surveillance colonoscopy: the Polyp Prevention Trial Continued Follow-up Study. Gastrointest Endosc 2010; 71: 111-117
- 16 Pabby A, Schoen RE, Weissfeld JL et al. Analysis of colorectal cancer occurrence during surveillance colonoscopy in the dietary Polyp Prevention Trial. Gastrointest Endosc 2005; 61: 385-391
- 17 Efthymiou M, Taylor ACF, Desmond PV et al. Biopsy forceps is inadequate for the resection of diminutive polyps. Endoscopy 2011; 43: 312-316
- 18 Draganov PV, Chang MN, Alkhasawneh A et al. Randomized, controlled trial of standard, large-capacity versus jumbo biopsy forceps for polypectomy of small, sessile, colorectal polyps. Gastrointest Endosc 2012; 75: 118-126
- 19 Vanagunas A, Jacob P, Vakil N. Adequacy of “hot biopsy” for the treatment of diminutive polyps: a prospective randomized trial. Am J Gastroenterol 1989; 84: 383-385
- 20 Gilbert DA, DiMarino AJ, Jensen DM et al. Status evaluation: hot biopsy forceps. American Society for Gastrointestinal Endoscopy. Technology Assessment Committee. Gastrointest Endosc 1992; 38: 753-756
- 21 Monkemuller KE, Fry LC, Jones BH et al. Histological quality of polyps resected using the cold versus hot biopsy technique. Endoscopy 2004; 36: 432-436
- 22 Ichise Y, Horiuchi A, Nakayama Y et al. Prospective randomized comparison of cold snare polypectomy and conventional polypectomy for small colorectal polyps. Digestion 2011; 84: 78-81
- 23 Horiuchi A, Nakayama Y, Kajiyama M et al. Removal of small colorectal polyps in anticoagulated patients: a prospective randomized comparison of cold snare and conventional polypectomy. Gastrointest Endosc 2014; 79: 417-423
- 24 Paspatis GA, Tribonias G, Konstantinidis K et al. A prospective randomized comparison of cold vs hot snare polypectomy in the occurrence of postpolypectomy bleeding in small colonic polyps. Colorectal Dis 2011; 13: 345-348
- 25 Bourke MJ. Making every colonoscopy count: Ensuring quality in endoscopy. J Gastroenterol Hepatol 2009; 24: S43-S50
- 26 Komeda Y, Suzuki N, Sarah M et al. Factors associated with failed polyp retrieval at screening colonoscopy. Gastrointest Endosc 2013; 77: 395-400
- 27 Rex DK, Alikhan M, Cummings O et al. Accuracy of pathologic interpretation of colorectal polyps by general pathologists in community practice. Gastrointest Endosc 1999; 50: 468-474
- 28 Pohl H, Srivastava A, Bensen SP et al. Incomplete polyp resection during colonoscopy – results of the complete adenoma resection (CARE) Study. Gastroenterology 2013; 144: 74-80
- 29 Konishi K, Kaneko K, Kurahashi T et al. A comparison of magnifying and nonmagnifying colonoscopy for diagnosis of colorectal polyps: a prospective study. Gastrointest Endosc 2003; 57: 48-53
- 30 Liu SL, Ho SB, Krinsky ML. Quality of polyp resection during colonoscopy: are we achieving polyp clearance?. Dig Dis Sci 2012; 57: 1786-179
Corresponding author
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References
- 1 Repici A, Hassan C, Vitetta E et al. Safety of cold polypectomy for < 10 mm polyps at colonoscopy: a prospective multicenter study. Endoscopy 2012; 44: 27-31
- 2 Tsai FC, Strum WB. Prevalence of advanced adenomas in small and diminutive colon polyps using direct measurement of size. Dig Dis Sci 2011; 56: 2384-2388
- 3 Ellis K, Schiele M, Marquis S et al. Efficacy of hot biopsy forceps, cold micro-snare and micro-snare with cautery techniques in the removal of diminutive colonic polyps. Gastrointest Endosc 1997; 45: 329-329
- 4 Humphris JL, Tippett J, Kwok A et al. Cold snare polypectomy for diminutive polyps: an assessment of the risk of incomplete removal of small adenomas. Gastrointest Endosc 2009; 69: AB207
- 5 Lee CK, Shim J-J, Jang JY. Cold snare polypectomy vs. cold forceps polypectomy using double-biopsy technique for removal of diminutive colorectal polyps: a prospective randomized study. Am J Gastroenterol 2013; 108: 1593-1600
- 6 Hyun-Soo K, Hye WonH, Hong JunP et al. Cold snare versus hot snare polypectomy for the complete resection of 5 – 9 mm sized colorectal polyps; A randomised controlled trial. Gastrointest Endosc 2014; 79: AB401-AB402
- 7 Pattullo V, Bourke MJ, Tran KL et al. The suction pseudopolyp technique: a novel method for the removal of small flat nonpolypoid lesions of the colon and rectum. Endoscopy 2009; 41: 1032-1037
- 8 Riley SA. Colonoscopic polypectomy and endoscopic mucosal resection: a practical guide. British Society of Gastroenterology. Available at: http://www.bsg.org.uk/images/stories/docs/sections/endo/polypectomy_08.pdf. Accessed 10 October 2014 2008
- 9 Hewett DG, Rex DK. Colonoscopy and diminutive polyps: hot or cold biopsy or snare? Do I send to pathology? . Clin Gastroenterol Hepatol 2011; 9: 102-105
- 10 Hewett DG. Colonoscopic polypectomy: current techniques and controversies. Gastroenterol Clin North Am 2013; 42: 443-458
- 11 NHS BCS Programme Pathology Group. Reporting lesions in the NHS Bowel Cancer Screening Programme. Guidelines from the Bowel Cancer Screening Programme Pathology Group. NHS BCSP publication no. 1. Sheffield, UK: NHS Cancer Screening Programmes; 2007
- 12 Fleiss JL. Measuring nominal scale agreement among many raters. Psychol Bull 1971; 76: 371-382
- 13 Altman DG. Practical statistics for medical research. London: Chapman and Hall; 1991
- 14 Farrar WD, Sawhney MS, Nelson DB et al. Colorectal cancers found after a complete colonoscopy. Clin Gastroenterol Hepatol 2006; 4: 1259-1264
- 15 Leung K, Pinsky P, Laiyemo AO et al. Ongoing colorectal cancer risk despite surveillance colonoscopy: the Polyp Prevention Trial Continued Follow-up Study. Gastrointest Endosc 2010; 71: 111-117
- 16 Pabby A, Schoen RE, Weissfeld JL et al. Analysis of colorectal cancer occurrence during surveillance colonoscopy in the dietary Polyp Prevention Trial. Gastrointest Endosc 2005; 61: 385-391
- 17 Efthymiou M, Taylor ACF, Desmond PV et al. Biopsy forceps is inadequate for the resection of diminutive polyps. Endoscopy 2011; 43: 312-316
- 18 Draganov PV, Chang MN, Alkhasawneh A et al. Randomized, controlled trial of standard, large-capacity versus jumbo biopsy forceps for polypectomy of small, sessile, colorectal polyps. Gastrointest Endosc 2012; 75: 118-126
- 19 Vanagunas A, Jacob P, Vakil N. Adequacy of “hot biopsy” for the treatment of diminutive polyps: a prospective randomized trial. Am J Gastroenterol 1989; 84: 383-385
- 20 Gilbert DA, DiMarino AJ, Jensen DM et al. Status evaluation: hot biopsy forceps. American Society for Gastrointestinal Endoscopy. Technology Assessment Committee. Gastrointest Endosc 1992; 38: 753-756
- 21 Monkemuller KE, Fry LC, Jones BH et al. Histological quality of polyps resected using the cold versus hot biopsy technique. Endoscopy 2004; 36: 432-436
- 22 Ichise Y, Horiuchi A, Nakayama Y et al. Prospective randomized comparison of cold snare polypectomy and conventional polypectomy for small colorectal polyps. Digestion 2011; 84: 78-81
- 23 Horiuchi A, Nakayama Y, Kajiyama M et al. Removal of small colorectal polyps in anticoagulated patients: a prospective randomized comparison of cold snare and conventional polypectomy. Gastrointest Endosc 2014; 79: 417-423
- 24 Paspatis GA, Tribonias G, Konstantinidis K et al. A prospective randomized comparison of cold vs hot snare polypectomy in the occurrence of postpolypectomy bleeding in small colonic polyps. Colorectal Dis 2011; 13: 345-348
- 25 Bourke MJ. Making every colonoscopy count: Ensuring quality in endoscopy. J Gastroenterol Hepatol 2009; 24: S43-S50
- 26 Komeda Y, Suzuki N, Sarah M et al. Factors associated with failed polyp retrieval at screening colonoscopy. Gastrointest Endosc 2013; 77: 395-400
- 27 Rex DK, Alikhan M, Cummings O et al. Accuracy of pathologic interpretation of colorectal polyps by general pathologists in community practice. Gastrointest Endosc 1999; 50: 468-474
- 28 Pohl H, Srivastava A, Bensen SP et al. Incomplete polyp resection during colonoscopy – results of the complete adenoma resection (CARE) Study. Gastroenterology 2013; 144: 74-80
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